Joint mouse–human phenome-wide association to test gene function and disease risk

Wang, Xusheng; Pandey, Ashutosh K.; Mulligan, Megan K.; Williams, Evan G.; Mozhui, Khyobeni; Li, Zhengsheng; Jovaisaite, Virginija; Quarles, L. Darryl; Xiao, Zhousheng; Huang, Jinsong; Capra, John A.; Chen, Zugen; Taylor, William L.; Bastarache, Lisa; Niu, Xinnan; Pollard, Katherine S.; Ciobanu, Daniel C.; Reznik, Alexander O.; Tishkov, Artem V.; Zhulin, Igor B.; Peng, Junmin; Nelson, Stanley F.; Denny, Joshua C.; Auwerx, Johan; Lu, Lu; Williams, Robert W.

doi:10.1038/ncomms10464

Title: Joint mouse–human phenome-wide association to test gene function and disease risk

Journal Article · Tue Feb 02 00:00:00 EST 2016 · Nature Communications

DOI:https://doi.org/10.1038/ncomms10464· OSTI ID:1327651

Wang, Xusheng ^[1]; Pandey, Ashutosh K. ^[2]; Mulligan, Megan K. ^[2]; Williams, Evan G. ^[3]; Mozhui, Khyobeni ^[2]; Li, Zhengsheng ^[2]; Jovaisaite, Virginija ^[3]; Quarles, L. Darryl ^[2]; Xiao, Zhousheng ^[2]; Huang, Jinsong ^[2]; Capra, John A. ^[4]; Chen, Zugen ^[5]; Taylor, William L. ^[2]; Bastarache, Lisa ^[4]; Niu, Xinnan ^[4]; Pollard, Katherine S. ^[6]; Ciobanu, Daniel C. ^[7]; Reznik, Alexander O. ^[8]; Tishkov, Artem V. ^[8];

^[8] more »

Univ. of Tennessee Health Science Center, Memphis, TN (United States); St. Jude Children's Research Hospital, Memphis, TN (United States)
Univ. of Tennessee Health Science Center, Memphis, TN (United States)
Ecole Polytechnique Federale de Lausanne, Lausanne (Switzlerland)
Vanderbilt Univ. School of Medicine, Nashville, TN (United States)
Univ. of California, Los Angeles, CA (United States)
Gladstone Institutes, San Francisco, CA (United States); Univ. of California, San Francisco, CA (United States)
Univ. of Tennessee Health Science Center, Memphis, TN (United States); Univ. of Nebraska, Lincoln, NE (United States)
Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
St. Jude Children's Research Hospital, Memphis, TN (United States)

Phenome-wide association is a novel reverse genetic strategy to analyze genome-to-phenome relations in human clinical cohorts. Here we test this approach using a large murine population segregating for ~5 million sequence variants, and we compare our results to those extracted from a matched analysis of gene variants in a large human cohort. For the mouse cohort, we amassed a deep and broad open-access phenome consisting of ~4,500 metabolic, physiological, pharmacological and behavioural traits, and more than 90 independent expression quantitative trait locus (QTL), transcriptome, proteome, metagenome and metabolome data sets-by far the largest coherent phenome for any experimental cohort (www.genenetwork.org). Here, we tested downstream effects of subsets of variants and discovered several novel associations, including a missense mutation in fumarate hydratase that controls variation in the mitochondrial unfolded protein response in both mouse and Caenorhabditis elegans, and missense mutations in Col6a5 that underlies variation in bone mineral density in both mouse and human.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1327651

Journal Information:: Nature Communications, Vol. 7; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 117 works

Citation information provided by
Web of Science

References (63)

Appearances can be deceiving: phenotypes of knockout mice Barbaric, I.; Miller, G.; Dear, T. N. Briefings in Functional Genomics and Proteomics, Vol. 6, Issue 2 https://doi.org/10.1093/bfgp/elm008	journal	September 2007
Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes Siepel, A. Genome Research, Vol. 15, Issue 8 https://doi.org/10.1101/gr.3715005	journal	August 2005
Antisense-induced exon skipping for duplications in Duchenne muscular dystrophy Aartsma-Rus, Annemieke; Janson, Anneke AM; van Ommen, Gert-Jan B. BMC Medical Genetics, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2350-8-43	journal	July 2007
Development of a Large-Scale De-Identified DNA Biobank to Enable Personalized Medicine Roden, Dm; Pulley, Jm; Basford, Ma Clinical Pharmacology & Therapeutics, Vol. 84, Issue 3 https://doi.org/10.1038/clpt.2008.89	journal	May 2008
Ten nucleotide differences, five of which cause amino acid changes, are associated with the Ah receptor locus polymorphism of C57BL/6 and DBA/2 mice Chang, Ching-yi; Smith, David R.; Prasad, V. S. Pharmacogenetics, Vol. 3, Issue 6 https://doi.org/10.1097/00008571-199312000-00005	journal	January 1993
Sensitive and accurate detection of copy number variants using read depth of coverage Yoon, S.; Xuan, Z.; Makarov, V. Genome Research, Vol. 19, Issue 9 https://doi.org/10.1101/gr.092981.109	journal	August 2009
Complex Trait Analysis of the Hippocampus: Mapping and Biometric Analysis of Two Novel Gene Loci with Specific Effects on Hippocampal Structure in Mice Lu, Lu; Airey, David C.; Williams, Robert W. The Journal of Neuroscience, Vol. 21, Issue 10 https://doi.org/10.1523/jneurosci.21-10-03503.2001	journal	May 2001
Transgenic overexpression of cardiac actin in the mouse heart suggests coregulation of cardiac, skeletal and vascular actin expression Kumar, A.; Crawford, K.; Flick, R. Transgenic Research, Vol. 13, Issue 6 https://doi.org/10.1007/s11248-004-2823-6	journal	December 2004
PLINK: A Tool Set for Whole-Genome Association and Population-Based Linkage Analyses Purcell, Shaun; Neale, Benjamin; Todd-Brown, Kathe The American Journal of Human Genetics, Vol. 81, Issue 3 https://doi.org/10.1086/519795	journal	September 2007
Aging: Seeking Mitonuclear Balance Karpac, Jason; Jasper, Heinrich Cell, Vol. 154, Issue 2 https://doi.org/10.1016/j.cell.2013.06.046	journal	July 2013
WebQTL: rapid exploratory analysis of gene expression and genetic networks for brain and behavior Chesler, Elissa J.; Lu, Lu; Wang, Jintao Nature Neuroscience, Vol. 7, Issue 5 https://doi.org/10.1038/nn0504-485	journal	May 2004
Detection of nonneutral substitution rates on mammalian phylogenies Pollard, K. S.; Hubisz, M. J.; Rosenbloom, K. R. Genome Research, Vol. 20, Issue 1 https://doi.org/10.1101/gr.097857.109	journal	October 2009
Inference of Population Structure Using Multilocus Genotype Data Pritchard, Jonathan K.; Stephens, Matthew; Donnelly, Peter Genetics, Vol. 155, Issue 2 https://doi.org/10.1093/genetics/155.2.945	journal	June 2000
Exome Sequencing of Ion Channel Genes Reveals Complex Profiles Confounding Personal Risk Assessment in Epilepsy Klassen, Tara; Davis, Caleb; Goldman, Alica Cell, Vol. 145, Issue 7 https://doi.org/10.1016/j.cell.2011.05.025	journal	June 2011
Multilayered Genetic and Omics Dissection of Mitochondrial Activity in a Mouse Reference Population Wu, Yibo; Williams, Evan G.; Dubuis, Sébastien Cell, Vol. 158, Issue 6 https://doi.org/10.1016/j.cell.2014.07.039	journal	September 2014
Systematic discovery of nonobvious human disease models through orthologous phenotypes McGary, K. L.; Park, T. J.; Woods, J. O. Proceedings of the National Academy of Sciences, Vol. 107, Issue 14 https://doi.org/10.1073/pnas.0910200107	journal	March 2010
Mitochondrial Stress Signals Revise an Old Aging Theory Woo, Dong Kyun; Shadel, Gerald S. Cell, Vol. 144, Issue 1 https://doi.org/10.1016/j.cell.2010.12.023	journal	January 2011
SIFT: predicting amino acid changes that affect protein function Ng, P. C. Nucleic Acids Research, Vol. 31, Issue 13 https://doi.org/10.1093/nar/gkg509	journal	July 2003
Germline mutations in FH predispose to dominantly inherited uterine fibroids, skin leiomyomata and papillary renal cell cancer Consortium, Multiple Leiomyoma Nature Genetics, Vol. 30, Issue 4, p. 406-410 https://doi.org/10.1038/ng849	journal	February 2002
Natural variation in genome architecture among 205 Drosophila melanogaster Genetic Reference Panel lines Huang, W.; Massouras, A.; Inoue, Y. Genome Research, Vol. 24, Issue 7 https://doi.org/10.1101/gr.171546.113	journal	April 2014
The Murine Family of Gut-Restricted Class Ib MHC Includes Alternatively Spliced Isoforms of the Proposed HLA-G Homolog, “Blastocyst MHC” Guidry, Paula A.; Stroynowski, Iwona The Journal of Immunology, Vol. 175, Issue 8 https://doi.org/10.4049/jimmunol.175.8.5248	journal	October 2005
Complex trait analysis of gene expression uncovers polygenic and pleiotropic networks that modulate nervous system function Chesler, Elissa J.; Lu, Lu; Shou, Siming Nature Genetics, Vol. 37, Issue 3 https://doi.org/10.1038/ng1518	journal	February 2005
Predicting phenotypic variation in yeast from individual genome sequences Jelier, Rob; Semple, Jennifer I.; Garcia-Verdugo, Rosa Nature Genetics, Vol. 43, Issue 12 https://doi.org/10.1038/ng.1007	journal	November 2011
The NAD+/Sirtuin Pathway Modulates Longevity through Activation of Mitochondrial UPR and FOXO Signaling Mouchiroud, Laurent; Houtkooper, Riekelt H.; Moullan, Norman Cell, Vol. 154, Issue 2 https://doi.org/10.1016/j.cell.2013.06.016	journal	July 2013
Mitochondria Are Required for Antigen-Specific T Cell Activation through Reactive Oxygen Species Signaling Sena, Laura A.; Li, Sha; Jairaman, Amit Immunity, Vol. 38, Issue 2 https://doi.org/10.1016/j.immuni.2012.10.020	journal	February 2013
Principles for the Buffering of Genetic Variation Hartman, John L.; Garvik, Barbara; Hartwell, Lee Science, Vol. 291, Issue 5506 https://doi.org/10.1126/science.1056072	journal	February 2001
Genetic Correlates of Gene Expression in Recombinant Inbred Strains: A Relational Model System to Explore Neurobehavioral Phenotypes Chesler, Elissa J.; Wang, Jintao; Lu, Lu Neuroinformatics, Vol. 1, Issue 4 https://doi.org/10.1385/ni:1:4:343	journal	January 2003
An Evolutionarily Conserved Role for the Aryl Hydrocarbon Receptor in the Regulation of Movement Williams, Evan G.; Mouchiroud, Laurent; Frochaux, Michael PLoS Genetics, Vol. 10, Issue 9 https://doi.org/10.1371/journal.pgen.1004673	journal	September 2014
Principles for the Buffering of Genetic Variation Hartman IV, J. L. Science, Vol. 291, Issue 5506 https://doi.org/10.1126/science.291.5506.1001	journal	February 2001
Opportunities for drug repositioning from phenome-wide association studies Rastegar-Mojarad, Majid; Ye, Zhan; Kolesar, Jill M. Nature Biotechnology, Vol. 33, Issue 4 https://doi.org/10.1038/nbt.3183	journal	April 2015
Mitonuclear protein imbalance as a conserved longevity mechanism Houtkooper, Riekelt H.; Mouchiroud, Laurent; Ryu, Dongryeol Nature, Vol. 497, Issue 7450 https://doi.org/10.1038/nature12188	journal	May 2013
The Cell-Non-Autonomous Nature of Electron Transport Chain-Mediated Longevity Durieux, Jenni; Wolff, Suzanne; Dillin, Andrew Cell, Vol. 144, Issue 1 https://doi.org/10.1016/j.cell.2010.12.016	journal	January 2011
Recent developments in the MAFFT multiple sequence alignment program Katoh, K.; Toh, H. Briefings in Bioinformatics, Vol. 9, Issue 4 https://doi.org/10.1093/bib/bbn013	journal	March 2008
PheWAS: demonstrating the feasibility of a phenome-wide scan to discover gene-disease associations Denny, J. C.; Ritchie, M. D.; Basford, M. A. Bioinformatics, Vol. 26, Issue 9 https://doi.org/10.1093/bioinformatics/btq126	journal	March 2010
Statistical significance for genomewide studies Storey, J. D.; Tibshirani, R. Proceedings of the National Academy of Sciences, Vol. 100, Issue 16, p. 9440-9445 https://doi.org/10.1073/pnas.1530509100	journal	July 2003
Systematic comparison of phenome-wide association study of electronic medical record data and genome-wide association study data Denny, Joshua C.; Bastarache, Lisa; Ritchie, Marylyn D. Nature Biotechnology, Vol. 31, Issue 12 https://doi.org/10.1038/nbt.2749	journal	November 2013
Pellino3 targets the IRF7 pathway and facilitates autoregulation of TLR3- and viral-induced expression of type I interferons Siednienko, Jakub; Jackson, Ruaidhri; Mellett, Mark Nature Immunology, Vol. 13, Issue 11 https://doi.org/10.1038/ni.2429	journal	October 2012
Pindel: a pattern growth approach to detect break points of large deletions and medium sized insertions from paired-end short reads Ye, K.; Schulz, M. H.; Long, Q. Bioinformatics, Vol. 25, Issue 21 https://doi.org/10.1093/bioinformatics/btp394	journal	June 2009
Slowed conduction and ventricular tachycardia after targeted disruption of the cardiac sodium channel gene Scn5a Papadatos, G. A.; Wallerstein, P. M. R.; Head, C. E. G. Proceedings of the National Academy of Sciences, Vol. 99, Issue 9 https://doi.org/10.1073/pnas.082121299	journal	April 2002
Surveillance-Activated Defenses Block the ROS–Induced Mitochondrial Unfolded Protein Response Runkel, Eva D.; Liu, Shu; Baumeister, Ralf PLoS Genetics, Vol. 9, Issue 3 https://doi.org/10.1371/journal.pgen.1003346	journal	March 2013
Discovering genotypes underlying human phenotypes: past successes for mendelian disease, future approaches for complex disease Botstein, David; Risch, Neil Nature Genetics, Vol. 33, Issue S3 https://doi.org/10.1038/ng1090	journal	March 2003
BreakDancer: an algorithm for high-resolution mapping of genomic structural variation Chen, Ken; Wallis, John W.; McLellan, Michael D. Nature Methods, Vol. 6, Issue 9 https://doi.org/10.1038/nmeth.1363	journal	August 2009
Mapping short DNA sequencing reads and calling variants using mapping quality scores Li, H.; Ruan, J.; Durbin, R. Genome Research, Vol. 18, Issue 11 https://doi.org/10.1101/gr.078212.108	journal	November 2008
Mouse genomic variation and its effect on phenotypes and gene regulation Keane, Thomas M.; Goodstadt, Leo; Danecek, Petr Nature, Vol. 477, Issue 7364 https://doi.org/10.1038/nature10413	journal	September 2011
Three Novel Collagen VI Chains with High Homology to the α3 Chain Gara, Sudheer Kumar; Grumati, Paolo; Urciuolo, Anna Journal of Biological Chemistry, Vol. 283, Issue 16 https://doi.org/10.1074/jbc.m709540200	journal	February 2008
System-wide molecular evidence for phenotypic buffering in Arabidopsis Fu, Jingyuan; Keurentjes, Joost J. B.; Bouwmeester, Harro Nature Genetics, Vol. 41, Issue 2 https://doi.org/10.1038/ng.308	journal	January 2009
Canalization of Gene Expression in the Drosophila Blastoderm by Gap Gene Cross Regulation PLoS Biology, Vol. 7, Issue 3, p. e1000049 https://doi.org/10.1371/journal.pbio.1000049	journal	March 2009
Systems Genetics of Metabolism: The Use of the BXD Murine Reference Panel for Multiscalar Integration of Traits Andreux, Pénélope A.; Williams, Evan G.; Koutnikova, Hana Cell, Vol. 150, Issue 6 https://doi.org/10.1016/j.cell.2012.08.012	journal	September 2012
A mitochondrial specific stress response in mammalian cells Zhao, Q. The EMBO Journal, Vol. 21, Issue 17 https://doi.org/10.1093/emboj/cdf445	journal	September 2002
Mitochondrial ROS Fire Up T Cell Activation Murphy, Michael P.; Siegel, Richard M. Immunity, Vol. 38, Issue 2 https://doi.org/10.1016/j.immuni.2013.02.005	journal	February 2013
A promoter polymorphism in the Per3 gene is associated with alcohol and stress response Wang, X.; Mozhui, K.; Li, Z. Translational Psychiatry, Vol. 2, Issue 1 https://doi.org/10.1038/tp.2011.71	journal	January 2012
A systematic, genome-wide, phenotype-driven mutagenesis programme for gene function studies in the mouse Nolan, Patrick M.; Peters, Jo; Strivens, Mark Nature Genetics, Vol. 25, Issue 4 https://doi.org/10.1038/78140	journal	August 2000
Needles in stacks of needles: finding disease-causal variants in a wealth of genomic data Cooper, Gregory M.; Shendure, Jay Nature Reviews Genetics, Vol. 12, Issue 9 https://doi.org/10.1038/nrg3046	journal	August 2011
Rescue of skeletal muscle α-actin–null mice by cardiac (fetal) α-actin Nowak, Kristen J.; Ravenscroft, Gianina; Jackaman, Connie The Journal of Cell Biology, Vol. 185, Issue 5 https://doi.org/10.1083/jcb.200812132	journal	May 2009
Flies give wings to human disease studies Todorovic, Vesna Nature Methods, Vol. 11, Issue 12 https://doi.org/10.1038/nmeth.3200	journal	November 2014
Unraveling the genetics and mechanisms of cardiac arrhythmia Noble, Denis Proceedings of the National Academy of Sciences, Vol. 99, Issue 9 https://doi.org/10.1073/pnas.102171699	journal	April 2002
A method and server for predicting damaging missense mutations Adzhubei, Ivan A.; Schmidt, Steffen; Peshkin, Leonid Nature Methods, Vol. 7, Issue 4 https://doi.org/10.1038/nmeth0410-248	journal	April 2010
Principles of Human Subjects Protections Applied in an Opt-Out, De-identified Biobank Pulley, Jill; Clayton, Ellen; Bernard, Gordon R. Clinical and Translational Science, Vol. 3, Issue 1 https://doi.org/10.1111/j.1752-8062.2010.00175.x	journal	February 2010
A Drosophila Genetic Resource of Mutants to Study Mechanisms Underlying Human Genetic Diseases Yamamoto, Shinya; Jaiswal, Manish; Charng, Wu-Lin Cell, Vol. 159, Issue 1 https://doi.org/10.1016/j.cell.2014.09.002	journal	September 2014
Treatment- and Population-Dependent Activity Patterns of Behavioral and Expression QTLs Ziebarth, Jesse D.; Cook, Melloni N.; Wang, Xusheng PLoS ONE, Vol. 7, Issue 2 https://doi.org/10.1371/journal.pone.0031805	journal	February 2012
Dioxin binding activities of polymorphic forms of mouse and human arylhydrocarbon receptors. Ema, M.; Ohe, N.; Suzuki, M. Journal of Biological Chemistry, Vol. 269, Issue 44 https://doi.org/10.1016/s0021-9258(18)46990-6	journal	November 1994
The Novel Cytokine p43 Stimulates Dermal Fibroblast Proliferation and Wound Repair Park, Sang Gyu; Shin, Hyosook; Shin, Young Kee The American Journal of Pathology, Vol. 166, Issue 2 https://doi.org/10.1016/s0002-9440(10)62262-6	journal	February 2005
Hurp Deficiency in Mice Leads to Female Infertility Caused by an Implantation Defect Tsai, Ching-Yen; Chou, Chen-Kung; Yang, Chu-Wen Journal of Biological Chemistry, Vol. 283, Issue 39 https://doi.org/10.1074/jbc.c800117200	journal	August 2008

Cited By (26)

Multi-omics analysis identifies ATF4 as a key regulator of the mitochondrial stress response in mammals Quirós, Pedro M.; Prado, Miguel A.; Zamboni, Nicola ETH Zurich https://doi.org/10.3929/ethz-b-000191490	text	January 2017
Identification of a Functional Non-coding Variant in the GABAA Receptor α2 Subunit of the C57BL/6J Mouse Reference Genome: Major Implications for Neuroscience Research Mulligan, Megan K.; Abreo, Timothy; Neuner, Sarah M. Frontiers in Genetics, Vol. 10 https://doi.org/10.3389/fgene.2019.00188	journal	March 2019
Diet modulates cecum bacterial diversity and physiological phenotypes across the BXD mouse genetic reference population Perez-Munoz, Maria Elisa; McKnite, Autumn M.; Williams, Evan G. PLOS ONE, Vol. 14, Issue 10 https://doi.org/10.1371/journal.pone.0224100	journal	October 2019
GenToS: Use of Orthologous Gene Information to Prioritize Signals from Human GWAS Hoppmann, Anselm S.; Schlosser, Pascal; Backofen, Rolf PLOS ONE, Vol. 11, Issue 9 https://doi.org/10.1371/journal.pone.0162466	journal	September 2016
Genetic Factors Mediate the Impact of Chronic Stress and Subsequent Response to Novel Acute Stress Terenina, Elena E.; Cavigelli, Sonia; Mormede, Pierre Frontiers in Neuroscience, Vol. 13 https://doi.org/10.3389/fnins.2019.00438	journal	May 2019
Systems genetics identifies a role for Cacna2d1 regulation in elevated intraocular pressure and glaucoma susceptibility Chintalapudi, Sumana R.; Maria, Doaa; Di Wang, Xiang Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00837-5	journal	November 2017
The expanded BXD family of mice: A cohort for experimental systems genetics and precision medicine Ashbrook, David G.; Arends, Danny; Prins, Pjotr BioRxiv https://doi.org/10.1101/672097	posted_content	July 2019
Genetic Regulation of Plasma Lipid Species and Their Association with Metabolic Phenotypes Jha, Pooja; McDevitt, Molly T.; Halilbasic, Emina Cell Systems, Vol. 6, Issue 6 https://doi.org/10.1016/j.cels.2018.05.009	journal	June 2018
GeneNetwork: A Toolbox for Systems Genetics Mulligan, Megan K.; Mozhui, Khyobeni; Prins, Pjotr Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-6427-7_4	book	December 2016
Ethanol-Induced Behavioral Sensitization Alters the Synaptic Transcriptome and Exon Utilization in DBA/2J Mice O’Brien, Megan A.; Weston, Rory M.; Sheth, Nihar U. Frontiers in Genetics, Vol. 9 https://doi.org/10.3389/fgene.2018.00402	journal	September 2018
Signaling and Regulation of the Mitochondrial Unfolded Protein Response Naresh, Nandhitha Uma; Haynes, Cole M. Cold Spring Harbor Perspectives in Biology, Vol. 11, Issue 6 https://doi.org/10.1101/cshperspect.a033944	journal	January 2019
Systems proteomics of liver mitochondria function Williams, Evan G.; Wu, Yibo; Jha, Pooja American Association for the Advancement of Science https://doi.org/10.5167/uzh-131608	text	January 2016
Multi-omics analysis identifies ATF4 as a key regulator of the mitochondrial stress response in mammals Quirós, Pedro M.; Prado, Miguel A.; Zamboni, Nicola Journal of Cell Biology, Vol. 216, Issue 7 https://doi.org/10.1083/jcb.201702058	journal	May 2017
The mitochondrial UPR: mechanisms, physiological functions and implications in ageing Shpilka, Tomer; Haynes, Cole M. Nature Reviews Molecular Cell Biology, Vol. 19, Issue 2 https://doi.org/10.1038/nrm.2017.110	journal	November 2017
The Genetic Basis of Baculum Size and Shape Variation in Mice Schultz, Nicholas G.; Ingels, Jesse; Hillhouse, Andrew G3: Genes\|Genomes\|Genetics, Vol. 6, Issue 5 https://doi.org/10.1534/g3.116.027888	journal	March 2016
Current Scope and Challenges in Phenome-Wide Association Studies Verma, Anurag; Ritchie, Marylyn D. Current Epidemiology Reports, Vol. 4, Issue 4 https://doi.org/10.1007/s40471-017-0127-7	journal	November 2017
Profiling DNA methylation differences between inbred mouse strains on the Illumina Human Infinium MethylationEPIC microarray Gujar, Hemant; Liang, Jane W.; Wong, Nicholas C. PLOS ONE, Vol. 13, Issue 3 https://doi.org/10.1371/journal.pone.0193496	journal	March 2018
Advanced Genetic Approaches in Discovery and Characterization of Genes Involved With Osteoporosis in Mouse and Human Yuan, Jinbo; Tickner, Jennifer; Mullin, Benjamin H. Frontiers in Genetics, Vol. 10 https://doi.org/10.3389/fgene.2019.00288	journal	April 2019
Quantifying and Localizing the Mitochondrial Proteome Across Five Tissues in A Mouse Population Williams, Evan G.; Wu, Yibo; Wolski, Witold American Society for Biochemistry and Molecular Biology https://doi.org/10.5167/uzh-162409	text	January 2018
Comparison and Functional Genetic Analysis of Striatal Protein Expression Among Diverse Inbred Mouse Strains Parks, Cory; Giorgianni, Francesco; Jones, Byron C. Frontiers in Molecular Neuroscience, Vol. 12 https://doi.org/10.3389/fnmol.2019.00128	journal	May 2019
Systems proteomics of liver mitochondria function Williams, E. G.; Wu, Y.; Jha, P. Science, Vol. 352, Issue 6291 https://doi.org/10.1126/science.aad0189	journal	June 2016
Profiling DNA Methylation Differences Between Inbred Mouse Strains on the Illumina Human Infinium MethylationEPIC Microarray Gujar, Hemant; Liang, Jane W.; Wong, Nicholas C. PLOS ONE https://doi.org/10.1101/194464	journal	September 2017
Fitting tissue chips and microphysiological systems into the grand scheme of medicine, biology, pharmacology, and toxicology Watson, David E.; Hunziker, Rosemarie; Wikswo, John P. Experimental Biology and Medicine, Vol. 242, Issue 16 https://doi.org/10.1177/1535370217732765	journal	June 2017
COL6A5 variants in familial neuropathic chronic itch Martinelli-Boneschi, Filippo; Colombi, Marina; Castori, Marco Brain https://doi.org/10.1093/brain/aww343	journal	January 2017
Genetic Dissection of Femoral and Tibial Microarchitecture Lu, Lu; Huang, Jinsong; Xu, Fuyi JBMR Plus, Vol. 3, Issue 12 https://doi.org/10.1002/jbm4.10241	journal	November 2019
Quantifying and Localizing the Mitochondrial Proteome Across Five Tissues in A Mouse Population Williams, Evan G.; Wu, Yibo; Wolski, Witold Molecular & Cellular Proteomics, Vol. 17, Issue 9 https://doi.org/10.1074/mcp.ra118.000554	journal	June 2018

Similar Records

Genetic dissection of bioenerrgy traits in sorghum

Technical Report · Fri Jun 15 00:00:00 EDT 2012 · OSTI ID:1327651

Vermerris, Wilfred; Kresovich, Stephen; Murray, Seth; +3 more

Shared Genomic Regions Underlie Natural Variation in Diverse Toxin Responses

Journal Article · Sat Oct 06 00:00:00 EDT 2018 · Genetics · OSTI ID:1327651

Evans, Kathryn S.; Brady, Shannon C.; Bloom, Joshua S.; +6 more

Genome-level analysis of genetic regulation of liver gene expression networks

Journal Article · Mon Jan 01 00:00:00 EST 2007 · Hepatology · OSTI ID:1327651

Gatti, Daniel; Maki, Akira; Chesler, Elissa J; +11 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Joint mouse–human phenome-wide association to test gene function and disease risk

Citation Formats

References (63)

Cited By (26)

Similar Records

Related Subjects